Broad receptor engagement of an emerging global coronavirus may potentiate its diverse cross-species transmissibility
Identifieur interne : 000D19 ( Pmc/Curation ); précédent : 000D18; suivant : 000D20Broad receptor engagement of an emerging global coronavirus may potentiate its diverse cross-species transmissibility
Auteurs : Wentao Li [Pays-Bas] ; Ruben J. G. Hulswit [Pays-Bas] ; Scott P. Kenney ; Ivy Widjaja [Pays-Bas] ; Kwonil Jung ; Moyasar A. Alhamo ; Brenda Van Dieren [Pays-Bas] ; Frank J. M. Van Kuppeveld [Pays-Bas] ; Linda J. Saif ; Berend-Jan Bosch [Pays-Bas]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2018.
Abstract
Coronaviruses exhibit a propensity for interspecies transmission, with SARS- and MERS-coronaviruses as notable examples. Cross-species transmission by coronaviruses is foremost determined by the virus’ ability to bind receptors of new hosts. We here report that the recently identified, yet globally distributed porcine deltacoronavirus employs host aminopeptidase N (APN) as an entry receptor via S protein-mediated interaction with an interspecies conserved domain that allows for APN orthologue-mediated entry. Identification of APN as a deltacoronavirus receptor emphasizes the remarkable preferential employment of cell surface host peptidases as receptors by coronaviruses. Our findings provide important insight into how receptor usage of coronaviruses may fuel cross-host transmission between distantly related species and necessitate surveillance studies of deltacoronaviruses in thus far unappreciated potential reservoirs, including humans.
Url:
DOI: 10.1073/pnas.1802879115
PubMed: 29760102
PubMed Central: 5984533
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Hulswit</name><affiliation wicri:level="1"><nlm:aff id="aff1">Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kenney, Scott P" sort="Kenney, Scott P" uniqKey="Kenney S" first="Scott P." last="Kenney">Scott P. 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Saif</name><affiliation><nlm:aff id="aff2">Department of Veterinary Preventive Medicine, Food Animal Health Research Program, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691</nlm:aff></affiliation></author><author><name sortKey="Bosch, Berend Jan" sort="Bosch, Berend Jan" uniqKey="Bosch B" first="Berend-Jan" last="Bosch">Berend-Jan Bosch</name><affiliation wicri:level="1"><nlm:aff id="aff1">Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29760102</idno><idno type="pmc">5984533</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5984533</idno><idno type="RBID">PMC:5984533</idno><idno type="doi">10.1073/pnas.1802879115</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">000D19</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000D19</idno><idno type="wicri:Area/Pmc/Curation">000D19</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000D19</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Broad receptor engagement of an emerging global coronavirus may potentiate its diverse cross-species transmissibility</title><author><name sortKey="Li, Wentao" sort="Li, Wentao" uniqKey="Li W" first="Wentao" last="Li">Wentao Li</name><affiliation wicri:level="1"><nlm:aff id="aff1">Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Hulswit, Ruben J G" sort="Hulswit, Ruben J G" uniqKey="Hulswit R" first="Ruben J. G." last="Hulswit">Ruben J. G. Hulswit</name><affiliation wicri:level="1"><nlm:aff id="aff1">Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kenney, Scott P" sort="Kenney, Scott P" uniqKey="Kenney S" first="Scott P." last="Kenney">Scott P. Kenney</name><affiliation><nlm:aff id="aff2">Department of Veterinary Preventive Medicine, Food Animal Health Research Program, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691</nlm:aff></affiliation></author><author><name sortKey="Widjaja, Ivy" sort="Widjaja, Ivy" uniqKey="Widjaja I" first="Ivy" last="Widjaja">Ivy Widjaja</name><affiliation wicri:level="1"><nlm:aff id="aff1">Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Jung, Kwonil" sort="Jung, Kwonil" uniqKey="Jung K" first="Kwonil" last="Jung">Kwonil Jung</name><affiliation><nlm:aff id="aff2">Department of Veterinary Preventive Medicine, Food Animal Health Research Program, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691</nlm:aff></affiliation></author><author><name sortKey="Alhamo, Moyasar A" sort="Alhamo, Moyasar A" uniqKey="Alhamo M" first="Moyasar A." last="Alhamo">Moyasar A. Alhamo</name><affiliation><nlm:aff id="aff2">Department of Veterinary Preventive Medicine, Food Animal Health Research Program, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691</nlm:aff></affiliation></author><author><name sortKey="Van Dieren, Brenda" sort="Van Dieren, Brenda" uniqKey="Van Dieren B" first="Brenda" last="Van Dieren">Brenda Van Dieren</name><affiliation wicri:level="1"><nlm:aff id="aff1">Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Van Kuppeveld, Frank J M" sort="Van Kuppeveld, Frank J M" uniqKey="Van Kuppeveld F" first="Frank J. M." last="Van Kuppeveld">Frank J. M. Van Kuppeveld</name><affiliation wicri:level="1"><nlm:aff id="aff1">Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Saif, Linda J" sort="Saif, Linda J" uniqKey="Saif L" first="Linda J." last="Saif">Linda J. Saif</name><affiliation><nlm:aff id="aff2">Department of Veterinary Preventive Medicine, Food Animal Health Research Program, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691</nlm:aff></affiliation></author><author><name sortKey="Bosch, Berend Jan" sort="Bosch, Berend Jan" uniqKey="Bosch B" first="Berend-Jan" last="Bosch">Berend-Jan Bosch</name><affiliation wicri:level="1"><nlm:aff id="aff1">Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Coronaviruses exhibit a propensity for interspecies transmission, with SARS- and MERS-coronaviruses as notable examples. Cross-species transmission by coronaviruses is foremost determined by the virus’ ability to bind receptors of new hosts. We here report that the recently identified, yet globally distributed porcine deltacoronavirus employs host aminopeptidase N (APN) as an entry receptor via S protein-mediated interaction with an interspecies conserved domain that allows for APN orthologue-mediated entry. Identification of APN as a deltacoronavirus receptor emphasizes the remarkable preferential employment of cell surface host peptidases as receptors by coronaviruses. Our findings provide important insight into how receptor usage of coronaviruses may fuel cross-host transmission between distantly related species and necessitate surveillance studies of deltacoronaviruses in thus far unappreciated potential reservoirs, including humans.</p></div></front></TEI><pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id><journal-id journal-id-type="hwp">pnas</journal-id><journal-id journal-id-type="pmc">pnas</journal-id><journal-id journal-id-type="publisher-id">PNAS</journal-id><journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title></journal-title-group><issn pub-type="ppub">0027-8424</issn><issn pub-type="epub">1091-6490</issn><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">29760102</article-id><article-id pub-id-type="pmc">5984533</article-id><article-id pub-id-type="publisher-id">201802879</article-id><article-id pub-id-type="doi">10.1073/pnas.1802879115</article-id><article-categories><subj-group subj-group-type="hwp-journal-coll"><subject>530</subject></subj-group><subj-group subj-group-type="heading"><subject>PNAS Plus</subject></subj-group><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Microbiology</subject></subj-group></subj-group><series-title>PNAS Plus</series-title></article-categories><title-group><article-title>Broad receptor engagement of an emerging global coronavirus may potentiate its diverse cross-species transmissibility</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Li</surname><given-names>Wentao</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Hulswit</surname><given-names>Ruben J. G.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kenney</surname><given-names>Scott P.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Widjaja</surname><given-names>Ivy</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jung</surname><given-names>Kwonil</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Alhamo</surname><given-names>Moyasar A.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>van Dieren</surname><given-names>Brenda</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>van Kuppeveld</surname><given-names>Frank J. M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Saif</surname><given-names>Linda J.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="corresp" rid="cor1"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bosch</surname><given-names>Berend-Jan</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1"><sup>2</sup></xref></contrib><aff id="aff1"><sup>a</sup>Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine,<institution>Utrecht University</institution>, 3584 CL Utrecht,<country>The Netherlands</country>;</aff><aff id="aff2"><sup>b</sup>Department of Veterinary Preventive Medicine, Food Animal Health Research Program, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691</aff></contrib-group><author-notes><corresp id="cor1"><sup>2</sup>To whom correspondence may be addressed. Email: <email>saif.2@osu.edu</email> or <email>b.j.bosch@uu.nl</email>.</corresp><fn fn-type="edited-by"><p>Contributed by Linda J. Saif, April 12, 2018 (sent for review February 15, 2018; reviewed by Tom Gallagher and Stefan Pöhlmann)</p></fn><fn fn-type="con"><p>Author contributions: W.L., R.J.G.H., S.P.K., I.W., L.J.S., and B.-J.B. designed research; W.L., R.J.G.H., S.P.K., I.W., K.J., M.A.A., and B.v.D. performed research; L.J.S. contributed new reagents/analytic tools; W.L., R.J.G.H., S.P.K., I.W., K.J., M.A.A., F.J.M.v.K., L.J.S., and B.-J.B. analyzed data; and R.J.G.H. and B.-J.B. wrote the paper.</p></fn><fn fn-type="con"><p>Reviewers: T.G., Loyola University Chicago; and S.P., German Primate Center.</p></fn><fn fn-type="equal" id="fn1"><p><sup>1</sup>W.L., R.J.G.H., and S.P.K. contributed equally to this work.</p></fn><fn fn-type="COI-statement"><p>The authors declare no conflict of interest.</p></fn></author-notes><pub-date pub-type="ppub"><day>29</day><month>5</month><year>2018</year></pub-date><pub-date pub-type="epub"><day>14</day><month>5</month><year>2018</year></pub-date><pub-date pub-type="pmc-release"><day>14</day><month>5</month><year>2018</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>115</volume><issue>22</issue><fpage>E5135</fpage><lpage>E5143</lpage><permissions><copyright-year>2018</copyright-year><license><ali:license_ref specific-use="vor">http://www.pnas.org/site/aboutpnas/licenses.xhtml</ali:license_ref><license-p>Published under the <ext-link ext-link-type="uri" xlink:href="http://www.pnas.org/site/aboutpnas/licenses.xhtml">PNAS license</ext-link>.</license-p></license></permissions><self-uri xlink:title="pdf" xlink:href="pnas.201802879.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Coronaviruses exhibit a propensity for interspecies transmission, with SARS- and MERS-coronaviruses as notable examples. Cross-species transmission by coronaviruses is foremost determined by the virus’ ability to bind receptors of new hosts. We here report that the recently identified, yet globally distributed porcine deltacoronavirus employs host aminopeptidase N (APN) as an entry receptor via S protein-mediated interaction with an interspecies conserved domain that allows for APN orthologue-mediated entry. Identification of APN as a deltacoronavirus receptor emphasizes the remarkable preferential employment of cell surface host peptidases as receptors by coronaviruses. Our findings provide important insight into how receptor usage of coronaviruses may fuel cross-host transmission between distantly related species and necessitate surveillance studies of deltacoronaviruses in thus far unappreciated potential reservoirs, including humans.</p></abstract><abstract><p>Porcine deltacoronavirus (PDCoV), identified in 2012, is a common enteropathogen of swine with worldwide distribution. The source and evolutionary history of this virus is, however, unknown. PDCoV belongs to the <italic>Deltacoronavirus</italic> genus that comprises predominantly avian CoV. Phylogenetic analysis suggests that PDCoV originated relatively recently from a host-switching event between birds and mammals. Insight into receptor engagement by PDCoV may shed light into such an exceptional phenomenon. Here we report that PDCoV employs host aminopeptidase N (APN) as an entry receptor and interacts with APN via domain B of its spike (S) protein. Infection of porcine cells with PDCoV was drastically reduced by APN knockout and rescued after reconstitution of APN expression. In addition, we observed that PDCoV efficiently infects cells of unusual broad species range, including human and chicken. Accordingly, PDCoV S was found to target the phylogenetically conserved catalytic domain of APN. Moreover, transient expression of porcine, feline, human, and chicken APN renders cells susceptible to PDCoV infection. Binding of PDCoV to an interspecies conserved site on APN may facilitate direct transmission of PDCoV to nonreservoir species, including humans, potentially reflecting the mechanism that enabled a virus, ancestral to PDCoV, to breach the species barrier between birds and mammals. The APN cell surface protein is also used by several members of the <italic>Alphacoronavirus</italic> genus. Hence, our data constitute the second identification of CoVs from different genera that use the same receptor, implying that CoV receptor selection is subjected to specific restrictions that are still poorly understood.</p></abstract><kwd-group><kwd>PDCoV</kwd><kwd>spike</kwd><kwd>APN</kwd><kwd>receptor</kwd><kwd>cross-species transmission</kwd></kwd-group><funding-group><award-group id="gs1"><funding-source id="sp1">ZonMw (Netherlands Organisation for Health Research and Development)<named-content content-type="funder-id">501100001826</named-content></funding-source><award-id rid="sp1">no.40-00812-98-13066</award-id></award-group></funding-group><counts><page-count count="9"></page-count></counts><custom-meta-group><custom-meta><meta-name>access-type</meta-name><meta-value>free</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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